science volume 324 issue 5923 2009 [doi 10.1126%2fscience.324.5923.28] pennisi, e. -- origins- on...
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8/9/2019 Science Volume 324 Issue 5923 2009 [Doi 10.1126%2Fscience.324.5923.28] Pennisi, E. -- OrIGINS- On the Origin of…
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IN 1879, CHARLES DARWIN PENNED A LETTER
to British botanist Joseph Dalton Hooker,
lamenting an “abominable mystery” that
threw a wrench into his theory of evolution:
How did flowering plants diversify and
spread so rapidly across the globe? From
rice paddies to orange groves, alpine mead-
ows to formal gardens, prairies to oak-hickory forests, the 300,000 species of
angiosperms alive today shape most terres-
trial landscapes and much of human life
and culture. Their blooms color and scent
our world; their fruits, roots, and seeds feed
us; and their biomass provides clothing,
building materials, and fuel. And yet this
takeover, which took place about 100 mil-
lion years ago, apparently happened in a
blink of geological time, just a few tens of
millions of years.
The father of evolution couldn’t quite
fathom it. Darwin had an “abhorrence that
evolution could be both rapid and poten-tially even saltational,” writes William
Friedman in the January American Journal
of Botany , which is devoted to this
“abominable mystery.” Throughout his life,
Darwin pestered botanists for their
thoughts on the matter, but they couldn’t
give him much help.
Now, 130 years later, evolutionary biol-
ogists are still pestering botanists for clues
about what has made this plant group so
successful, as well as when, where, and
how flowers got started—and from which
ancestor. Today, researchers have analytical
tools, fossils, genomic data, and insights that
Darwin could never have imagined, all of
which make these mysteries less abom-
inable. Over the past 40 years, techniques
for assessing the relationships between
organisms have greatly improved, and gene
sequences, as well as morphology, now help
researchers sort out which angiosperms
arose early and which arose late. New fossil
finds and new ways to study them—with
synchrotron radiation, for example—pro-
vide a clearer view of the detailed anatomy
of ancient plants. And researchers from var-ious fields are figuring out genomic changes
that might explain the amazing success of
this fast-evolving group.
These approaches have given researchers
a much better sense of what early flowers
were like and the relationships among them.
But one of Darwin’s mysteries remains: the
nature and identity of the angiosperm ances-
tor itself. When flowering plants show up in
the fossil record, they appear with a bang,
with no obvious series of intermediates, as
Darwin noted. Researchers still don’t know
which seed- and pollen-bearingorgans eventually evolved into
the comparable flower parts.
“We’re a bit mystified,” says
botanist Michael Donoghue of
Yale University. “It doesn’t
appear that we can locate a close
relative of the flowering plants.”
Seeking the first flowerOne of two major living groups
of seed plants, angiosperms have
“covered” seeds that develop
encased in a protective tissue
called a carpel (picture a bean pod). That’s in contrast to the
nonflowering gymnosperms,
such as conifers, which bear
naked seeds on scales. An
angiosperm’s carpel sits at the
center of the flower, typically
surrounded by pollen-laden sta-
mens. In most flowers, the carpel and stamens
are surrounded by petals and an outer row of
leaflike sepals. Seeds have a double coating
as well as endosperm, tissue surrounding the
embryo that serves as its food supply.
Darwin was perplexed by the diversity
flowering plants; they were too numerou
and too varied, and there were too few fo
sils to sort out which were more primitiv
Throughout much of the 20th century, ma
nolia relatives with relatively large flowe
were leading candidates for the most prim
tive living flowers, although a fe
researchers looked to small herbs instead.
In the late 1990s, molecular systemati
came to the rescue, with several reports pr
senting a fairly consistent picture of th
lower branches of the angiosperm tree. A
obscure shrub found only in New Caledon
emerged as a crucial window to the pas
Amborella trichopoda, with its 6-millimet
greenish-yellow flowers, lives deep in th
cloud forests there. In multiple gene-base
assessments, including an analysis in 200
of 81 genes from chloroplast genome
belonging to 64 spec ies, Amborel la si
at the base of the angiosperm family trethe sister group of all the rest of th
angiosperms.
Given that placement, Amborella’s tin
flowers may hint at what early blossom
were like. It’s one of “the most similar livin
flower[s]” to the world’s first flower, say
James Doyle of the University of Califo
nia, Davis. The petals and sepals of its sin
gle-sex flowers are indistinguishable an
vary in number; so too do the numbers
seed-producing carpels on female flowe
and pollen-generating stamens on ma
flowers. The organs are spiralarranged, and carpels, rath
than being closed by fused ti
sue as in roses and almost a
familiar flowers, are sealed by
secretion.
Most genetic analyses showe
that water lilies were the ne
branch up the angiosperm tre
followed by a group represente
by star anise, which also has
pr imit ive lo ok ab ou t it , say
Doyle, “though each of the
has deviations from the ance
tral type.”
Fossil recordsAlthough some fossil polle
dates back 135 million years, n
credible earlier fossil evidenc
exists. In Darwin’s day, and f
many decades afterward, pal
obotanists primarily found leaves or polle
but almost no fossil flowers. They had th
wrong search image, says Else Marie Friis
the Swedish Museum of Natural History
On the Origin of
Flowering Plants
8 3 APRIL 2009 VOL 324 SCIENCE www.sciencemag.org
THE YEAR OF
This essay is the fourthin a monthly series.
For more on evolutionarytopics online, see theOrigins blog atblogs.sciencemag.org/origins. For more onflower origins, listento a podcast by authorElizabeth Pennisi atwww.sciencemag.org/multimedia/podcast.
DARWIN
NEWSFOCUS
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ORIGINS
Stockholm. “When we started,
the search profile was bigger,
a magnolia [flower],” she
recalls. But 30 years ago, she
and others discovered tiny
ancient flowers by sieving
through sand and clay sedi-
ments. With this technique,
they have now collected hun-
dreds of millimeter-size
flowers, some preserved in
three dimensions, from Por-
tugal and other locations with
Cretaceous deposits 70 mil-
lion to 120 million years old.
This fossil diversity
shows that angiosperms were
thriving, with several groups
well-established, by 100 mil-
lion years ago. In some, the
flower parts are whorled like
those of modern flowers; in
others they are spiraled, con-sidered by some researchers
as the more primitive arrangement. Some
flower fossils have prescribed numbers of
petals, another modern feature, whereas in
others the petal count varies.
In 1998, Chinese geologist Ge Sun of
Jilin University in Changchun, China, came
across what seemed to be a much older
flower. The fossil, called Archaefructus, was
an aquatic plant that looked to be 144 mil-
lion years old. By 2002, Sun and David
Dilcher of the Florida Museum of Natural
History (FLMNH) in Gainesville had described an entire plant, from roots to flow-
ers, entombed on a slab of rock unearthed in
Liaoning in northeastern China.
In one sense, Archaefructus wasn’t much
to look at. “It’s a flowering plant befo re
there were flowers,” Dilcher notes. It lacked
petals and sepal s, but it did have an
enclosed carpel. When Kevin Nixon and
colleagues at Cornell University compared
its traits with those same traits in 173 living
plants, Archaefructus came out as a sister to
living angiosperms and closer to the com-
mon ancestor than even Amborella.
Archaefructus’s distinction was short-lived, however. Within months, better dat-
ing of the sediments in which it was found
yielded younger dates, putting this first
flower squarely with other early fossil
flower parts, about 125 million years old.
Also, a 2009 phylogenetic analysis of
67 taxa by Doyle and Peter Endress of the
University of Zurich, Switzerland, placed
the fossil in with water lilies rather than at
the base of the angiosperms, although this
conclusion is contested.
These fossils often spark debate because
specimens tend to be imperfectly preserved
and leave room for interpretation. To help
remedy that, Friis and her colleagues have
begun to examine flowers using synchro-
tron radiation to generate a 3D image of
their inner structures, allowing the fossil to
remain intact while Friis peers inside it
from many angles (Science, 7 December
2007, p. 1546). “We can get fantastic reso-
lution,” says Friis. “It’s really exciting.” But
so far, the flowers Friis finds are
too diverse to trace back to a pa rti cu la r ance stor. “Fro m
these fossils, we cannot
say what is the basic
form,” she says.
Before flowers
Although they have yet
to find the oldest fossil
flowers, researchers
assume that the ances-
tral angiosperm evolved
from one of the nonflowering seed plan
or gymnosperms, whose heyday was 20
million years ago. Modern gymnosperm
include conifers, ginkgoes, and the cycad
with their stout trunks and large frond
Before angiosperms came along, thes
plants we re much more div erse an
included cycadlike species, such as th
extinct Bennettitales, and ma ny wood
plants cal led Gnetales, of wh ic
a few representatives, including th
joint firs, survive today (see family tre p. 31). Also common in the Jurassic we
seed ferns, a g roup now long gone; the
most famous member is Caytonia, whic
seems to have precarpel-like structure
These groups’ perceived relevance
flower evolution and their relationships
angiosperms have ping-ponged betwee
camps, depending on how the evolutionar
trees were constructed.
In the mid-1980s, Peter Crane, now
the University of Chicago in Illinois, pr
posed a solution, the anthophyte hypothesi
Using several lines of evidence and notin
that both Bennettitales anGnetales organize their ma
and female organs togeth
in what could be con
strued as a preflowe
he considered them
along with angiosperm
as comprising a sing
angiosperm entity calle
anthophytes. For the ne
decade, most family tre
based on morphology sup
Out of the past.
Tiny Amborella sits
at the bottom of the
angiosperm family tree.
www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009
“We are realizing that this
huge diversity is probably
the result of one innova-
tion piled on top of
another innovation.” — Peter Crane,
University of Chicago
C R E D I T S ( T O P T O B O T T O M ) : C O U R T E S Y O F S T E P H E N
M C C A B E , U C S A N T A C R U Z ; P H O T O B Y J E N N I F E R S V I T K O , C O U
R T E S Y O F W I L L I A M L . C R E P E T , C O R N E L L U N I V E R S I T Y
Larger than life. Although merely
2.2 millimeters in diameter, this 3D
fossil flower shows that grasses date
back to 94 million years ago.
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3/4
ported this idea. Crane and others carefully
dissected and described fossils of these
groups, looking for the precursors to
carpels, the seed’s double coat, and other
distinctive angiosperm traits.
But they have run into problems. “We do
not really know how to compare them
because the s tructures are very different-
looking; figuring out what’s homologous isquite a diff icult thing,” says Crane. He and
his colleagues argue, for example, that the
seeds in the Bennettitales have two cover-
ings, which may be a link to angiosperms.
But in the January American Journal of
Botany, Gar Rothwell of Ohio University,
Athens, and two colleagues disagree, say-
ing that what Crane calls the outer layer is
the only layer, and find
fault with the hypothesis
in general.
To make matte rs
worse for anthophyte
propone nts, gene- bas ed evol ut io nar y
trees break up this
grouping, pulling the
Gnetales off any
angiosperm branch
and placing them
among or next to the
other gymnosperms.
“The molecular work
points in one dire c-
tion; the paleobotanical
work points you in another direction,”
Crane says.
And if the molecular work is correct,
then the f ield doesn’t know in which direc-
tion to turn, because in most analyses the
genetic data don’t place any living plant
close to angiosperms. The angiosperms
group together, the living gymnosperms
group togethe r, and there’s nothing in between. “The nonangiosperm ancestor just
isn’t there,” says paleobotanist William
Crepet of Cornell. “I’m starting to worry
that we will never know, that it transformed
without intermediates.”
Seeds of success
The angiosperm’s ancestor may be missing,
but what is ve ry cl ea r—a nd was qu it e
annoying to Darwin—is that the angio-
sperm prototype so readily proved a
winner. Seed ferns and
other gymnosperms
arose about 370million years ago
and dominated the
planet for 250 mil -
lion years. Then in a
few tens of millions
of years, angio-
sperms edged them
out. Today, almost nine in 10 land plan
are angiosperms.
The exact timing of the angiosperm
explosion and expansion is under debate, as
the cause. At least one estimate based on th
rate at which gene sequences change—th
is, the ticking of the molecular clock—
pushes angiosperm evolution back to 21
million years ago. “There appears to begap in the fossil record,” says Donoghu
who also notes that molecular dating meth
ods “are still in their infancy” and, thu
could be misleading. He and others thin
that flowering plants lingered in obscuri
for tens of millions of years before radiatin
toward their current diversity.
Whatever the timing, there was som
thing special about the angiosperm radi
tion. During the 1980s and again in 199
Cornell’s Karl Niklas compiled a databa
showing the f irst and last occurrences
fossil plants. When he and Crepet used th
and more recent information to look species’ appearances and disappearance
they found that new angiosperms appeare
in bursts through time, whereas other plant
such as gymnosperms, radiated rapidly on
at first. Moreover, angiosperms proved le
likely to disappear, somehow resistin
extinction, says Crepet.
Once the angiosperms arrived, how d
they diversify and spread so quickly? Darw
suspected that coevolution with insect poll
nators helped drive diversification, thoug
0 3 APRIL 2009 VOL 324 SCIENCE www.sciencemag.org
Flowers, food, fuel. Darwin marveled at the diversity of angiosperms. Giventhat they represent nine in 10 land plants, it’s no surprise that they serve as
mainstays of both our welfare and sense of beauty. Clockwise from left: aspenorchids, grasses, sunflowers, tulips, apples, walnuts.
ORIGINS
Inside and out. Synchrotron radiation helped pro-duce a 3D rendering (gold) of this fossil male flower(right ) and insights into its internal structure.
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C R E D I T S : ( A R C H A E F R U C T U S I M A G E ) D A V I D D I L C H E R ;
( A L L O T H E R I M A G E S ) P H O T O S . C
O M
such a causal relationship is not set-
tled. Later, animals that ate fruit and
dispersed seeds likely helped evolv-
ing species expand quickly into new
territory. Some think the answer lies
in genes: duplications that gave the
angiosperm genome opportunities to
try out new floral shapes, new chem-
ical attractants, and so forth. This
flexibility enabled angiosperms to
exploit new niches and set them up
for long-term evolutionary success.
“My own view is that in the past, we
have looked for one feature,” says
Crane. Now, “we are realizing that
this huge diversity is probably the
result of one innovation piled on top
of another innovation.”
The latest insights into diversifica-
tion come from gene studies. From
2001 to 2006, Pamela Soltis of the
FLMNH and Claude dePamphilis
of Pennsylvania State University,University Park, participated in
the Floral Genome Project, which
searched for genes in 15 angiosperms.
Now as a follow-up, the Ancestral
Angiosperm Genome Project looks
at gene activity in five early angio-
sperms and a cycad, a gymnosperm.
DePamphilis and his colleagues
matched all the genes in each
species against one another to deter-
mine the number of duplicates. They
then looked at the number of differ-
ences in the sequences of each gene pair to get a sense of how long ago
the duplication occurred. In most
early angiosperms, including water
lilies and magnolias, they saw many
simultaneous duplications—but not
in Amborella , they reported in the
January 2009 American Journal of Botany,
confirming earlier reports. The data suggest
that a key genome duplication happened
after the lineage leading to Amborella split
off but before water lilies evolved. “We’re
beginning to get the idea that polyploidiza-
tion may have been a driving force in creat-
ing many new genes that drive floral devel-opment,” dePamphilis says.
Others have noted that a duplication
occurred in the evolution of grasses, and the
Floral Genome Project confirms that yet
another duplication paved the way for eudi-
cots, the group that includes apples, roses,
beans, tomatoes, and sunflowers. “There are
some real ‘hot spots’ in angiosperm evolu-
tionary history,” says dePamphilis, who is
working to fully sequence the genome of
Amborella with his colleagues.
The Floral Genome Project also looked
to see whether the genetic programs guiding
flower development were consistent
throughout the angiosperms. “We found that
there are fundamental aspects that are con-
served in the earliest lineages,” says Soltis.
“But there are differences in how the genes
are deployed.”Take the avocado, a species on the lower
branches of the angiosperm tree. In most
angiosperms, the flower parts are arranged in
concentric circles, or whorls, around the
carpels, with stamens innermost, then petals,
and finally sepals. Each tissue has its own
distinct pattern of gene expression, but not
in the avocado. Genes that in Arabidopsis
are active only in, say, the developing petals
spill over in avocado to the sepals. Thus in
the more primitive plants, petals and sepals
are not as well-defined as they are in Ar
bidopsis. This sloppiness may have mad
development flexible enough to underg
many small changes in expression pattern
and functions that helped yield the gre
diversity in floral forms.
In his letter to Hooker, Darwin wro
that he would like “to see this whole problem solved.” A decade ago, Crepet thoug
Darwin would have gotten his wish by now
That hasn’t happened, but Crepet is opt
mistic that he and his colleagues are on th
right track, as analyses of various kinds
data become more sophisticated. “We a
less likely to go around in circles in the ne
10 years,” he says. “I believe a solution t
the problem is within reach. … The myster
is solvable.”
–ELIZABETH PENNI
Paleozoic seed ferns
Archaefructus
Caytonia
Bennettitales
Asterids
Rosids
Eudicots
Monocots
Magnolias
Water lilies
Cycads
Ginkgoes
Gnetales
Conifers
Amborella
A n gi o s p e r m s
L i v i n g
g y mn o s p e r m s
Extinct taxa
SEED PLANT
PHYLOGENY
»
»
»
»
»
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Shifting branches. As this simplified family tree shows, gene studies have helped clarify the relationships of ma
living angiosperms, but fitting in extinct species is still a challenge, and some nodes are hotly debated.
ORIG
P bli h db AAAS
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